Seasonal variations and changes in the diet of southern river otter in different freshwater habitats in Chile
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1 Acta Theriologica 43 (3): , PL ISSN Seasonal variations and changes in the diet of southern river otter in different freshwater habitats in Chile Gonzalo MEDINA Medina G Seasonal variations and changes in the diet of southern river otter in different freshwater habitats in Chile. Acta Theriologica 43: The diet of southern river otter Lutra prouocax Thomas, 1908 was determined from 605 scats collected from four sites in Southern Chile between Crustacean remains were the most common item found in scats. Crustacean species that were the most common in scats collected from lakes, became less important in the river outlets. Fish remains were all from fish less than 100 mm in length and were found more frequently in scats collected at the river sites than at the lake sites. Differences in the diet between otter's scats collected in lakes and their river outlets may be related to prey availability and vulnerability. Diet was more diverse in river habitats than in the lakes. The diet of southern river otter appears to be closer to that described for Aonyx capensis and Lutra maculicollis in South Africa. The southern river otter is heavily dependent on the abundance of three crustacean species. Differences in the diets observed between lake and their river outlets suggest important differences in habitat conditions. This may have future implications for prioritising habitat protection in the conservation of southern river otter. Instituto de Ecología y Evolución, Universidad Austral de Chile, Casilla 567, Valdivia, Chile, gmedina@uach.cl Key words: Lutra prouocax, diet, rivers, lakes, crustaceans Introduction Food studies on Lutra lutra in Europe and Lutra canadensis in North America indicate that in freshwater habitats these otters are primarily piscivorous (Melquist and Hornocker 1983, Mason and Macdonald 1986). In contrast, studies of the feeding habits of southern river otter in freshwater habitats in Chile and Argentina suggest that crustaceans and mussels are the most important dietary component (Chehebar 1985, Chehebar et al. 1986, Medina 1991, Medina 1997). However, there is a lack of information about the effects of different habitat conditions and seasons on the diet of the southern river otter. This research provides insights into the variations of the diet of southern river otter between lakes and rivers, seasons and size of prey. [285]
2 286 G. Medina Study area and methods Two lakes and their main river outlets were chosen for this study (Fig. 1), representing two of the remaining regions holding southern river otter populations in freshwater habitat in Chile (Medina 1996). Lake Panguipulli (39 43' S, 72 13' W) is drained by the Enco River (140 m a.s.l.) (Fig. 1). The lake is oligotrophic with temperatures above 4 C and a maximum surface temperature of 21"C (Campos et al. 1981). Potential otter prey in Lake Panguipulli and Enco River include the introduced trout Oncorhynchus mykiss ( mm length) and Salmo trutta ( mm); the native fishes Aplochiton zebra ( mm length, average 71 mm), Trichomycterus areolatus ( mm length, average 52 mm), Percilia gillissi (26-64 mm length, average 42 mm), Galaxias platei, Diplomystes chilensis, and Percichthys trucha ( mm length); the crabs Aegla rostrata (21-45 mm cephalotorax length), Aegla abtao, Aegla denticulata (8-37 mm cephalotorax length), the crayfish Samastacus spinifrons; and the mussels Diplodon chilensis and Chilina spp. (Jara 1977, 1989, Campos 1985, C. G. Jara, pers. comm.). The lake shoreline is mainly steep and rocky, 23% of its surface area is of shallow zones (< 30 m deep) (Campos et al. 1981). The Enco River is the only outlet for Lake Panguipulli (Fig. 1), with a rocky shoreline covered with abundant vegetation (eg, Chusquea quila, Notofagus dombeyi). Lake Todos los Santos (41 08' S, 72 12' W) is drained by the Petrohue River (Fig. 1) (189 m a.s.l.). The lake is oligotrophic with temperatures above 8 C and a maximum surface temperature of 19 C (Campos et al. 1990). Potential otter preys are the same as in Lake Panguipulli and the Enco River except that Aegla denticulata is absent (Campos 1985, Jara 1977, 1989, C. G. Jara, pers. comm.). The lake shoreline is steep and rocky and is covered with abundant vegetation (in particular Amomyrtus luma, Myrceugenia exsucca, Luma apiculata, Drimys winteri and Nothofagus 19' PANGUIPULLI tí TODOS LOS SANTOS CHILE 56' ENCO RIVER 0 5 km Fig. 1. Geographic location of the study areas and sites ( ) where otter scats were collected.
3 Southern river otter diet in Chile 287 dombeyi), 8% of the lake surface area is of shallow zones (< 30 m deep) (Campos et al. 1990). The Petrohué River (Fig. 1) is the only outlet for the lake, with a steep, rocky shoreline also covered with abundant vegetation (Nothofagus spp.). From August 1990 to November 1991 monthly patrols were made on foot or by canoe along the shorelines of the study sites. During the initial survey only otter dens and rest-sites were located. Fresh otter scats (one month old or less) were collected monthly in or between dens and rest-sites that were earlier identified (Fig. 1). Scats were dried at 75 C for 24 to 48 hours (Bagenal 1978) and stored in paper bags for later analysis. Prey remains in the dried scats were identified and compared with reference material held at the Instituto de Ecología y Evolución, Universidad Austral de Chile. Fish remains in collected otter scats were identified using scales operculae and vertebrae, and their size estimated by comparing the size of abdominal and caudal vertebrae with previously measured reference material (adapted from Wise 1980). Fish were classified into eight length categories (< 39 mm, mm, mm, mm, mm, mm, mm, > 100 mm). The results were tabulated as occurrence (number of scats in which a species occurred), frequency of occurrence (number of scats in which a species occurred divided by the total number of scats collected) and relative frequency (number of scats in which a species occurred divided by the total occurrence of all the species tested) (Erlinge 1968, Rowe-Rowe 1977, Medina 1997). These were tested as arcsine- -transformed frequencies of occurrence. Seasonal variation of prey categories and species in otter scats at the same lake and river were assessed by Friedman two-way ANOVA. Correlations of monthly frequency of occurrence between prey species and between prey categories at the same lake or river were determine by linear regression. Comparison of the mean frequencies of occurrence of prey species and categories between lakes and their river outlets were made using Wilcoxon signed rank (Berenson et al. 1988). Differences between fish size categories were evaluate by two-way ANOVA and pairwise compared using Fisher's Least-Significant-Difference Test (LSD). Prey diversity in the diet was assessed using the Shannon-Wiener diversity index (Krebs 1989) and the indexes were compared using Hutcheson's -test method (Magurran 1988). Results Diet composition Crustaceans were the most frequently found prey in the 605 otter scats collected followed by fish. Mussels and birds were rarely recorded (Table 1). At most sites there were no seasonal changes in the diet (Fig. 2) except at Enco River, where P. trucha recorded a significant seasonal change towards spring and summer (F3,8 = 13.5, p < 0.05). There was no correlation between prey species and between prey categories. Fish size In otter scats a total of 127 fish remains for lakes and 98 for rivers were measured to estimate fish size. Fish eaten by otters were all less than 100 mm in length with no overall significant difference between the size categories. However, the frequency offish size between 80 and 99 mm length was a significant less than the frequency of fish between 40 and 49 mm length (Table 2). Also, no significant difference was recorded between fish size estimated from remains found in scats collected at lakes and scats collected at river habitats (Table 2).
4 288 G. Medina Table 1. Occurrence (O) and frequency of occurrence (FO) of prey species and category in otter scats collected in the study lakes (L) and rivers (R), n - indicate number of scats collected. L. Panguipulli Prey species ( n = ^42) Eneo R. L. T. Los Santos Petrohué R. (n = 86) (n = 217) (n = 60) O FO O FO O FO O FO Total crustaceans Aegla rostrata Aegla abtao abtao Samastacus spinifrons Total fish Percilia gillissi Percichthys trucha Oncorhynchus mykiss Salmo trutta Galaxias spp Undetermined Total mussels Chilina spp Total birds Podilymbus podiceps Total Table 2. Fish size relative frequency (%) in otter scats collected at the studied lakes (L) and rivers (R). Fish length categories with the same letter differ significantly (Fisher's LSD: p < 0.03). Species Fish length (mm) Percilia Perachthys Oncorhynchus Salmo categories gillissi trucha mykiss trutta L R L R L R L R L R 0 < 39 a b c d e f, b g, b Sample size
5 Southern river otter diet in Chile j I -- Crustaceans Fish j o r 1 ' u c_ o c O O 1.5 j S' a Fig. 2. Seasonal frequency of occurrence of fish and crustaceans in otter scats collected at (a) - Lake Panguipulli (n = 242), (b) - Enco river (n = 86), (c) - Lake Todos los Santos (n = 217), and (d) - Petrohué river (n = 60). 1.5 j autumn winter spring Seasons Comparisons between the study sites The monthly frequencies of occurrence of A. abtao and A. rostrata were of significant difference between the scats collected in lakes and their river outlets (Lake Panguipulli vs Enco River; Wilcoxon: Z = 2.9, p < 0.05; Z = 3.0, p < 0.05 respectively) and A. abtao and S. spinifroms (Lake Todos los Santos vs Petrohue river; Wilcoxon: Z = 2.8, p < 0.05; Z = 3.0, p < 0.05 respectively). Furthermore, there was a switch from the most important crustacean prey species between lakes and their river outlets (Table 1). The crustacean prey species that were the most important at lakes became less important at the river outlets. Significant differences in the monthly frequency of occurrence to the introduced trouts between Lake Panguipulli and Enco river (Wilcoxon: Z = 2.1, p < 0.05), and Lake Todos los Santos and Petrohue river (Wilcoxon: Z = 3.0, p < 0.05) were also recorded. Fish remains were significantly (Wilcoxon: Z = 4.6, p < 0.05) more frequent in scats collected at the rivers than at the lake sites. All prey species recorded were equally represented by their occurrences in the scats collected from the river outlets (larger Even and H' indices) more than those collected from the lakes (Table 3).
6 290 G. Medina Table 3. Diet diversity indices assessed from river otter scats obtained in two Chilean lakes and two rivers. H' - Diversity index (Shannon and Weaver 1963), N - number of groups of scats tes:ed, H'Max - Maximum diversity, VarH' - Variance, Even - Evenness. All H' are significantly different (p < 0.05). Study areas N H' H'Max VarH' Even Lake Panguipulli Enco river Lake T. Los Santos Petrohué river Discussion Food preference Although, crustaceans have been described as a lower quality food for otter than that of fish (Kruuk 1995), this study shows that southern river otter is heavily dependent on the abundance of three crustacean species. This differs from L. lutra in Europe and L. canadensis in North America where diets in aquatic habitats are primarily piscivorous (Melquist and Hornocker 1983, Mason and Macdonald 1986). Therefore, the feeding strategy of the southern river otter appears to be closer to that of the African species A. capensis and L. maculicollis, which predate highly on crabs where freshwater habitats have poor fish faunas (Rowe-Rowe 1977, 1991, Lejeune 1990). L. lutra and L. canadensis rarely prey on fish less than 100 mm in length (Toweill 1974, Jenkins and Harper 1980, Wise et al. 1981, Adrian and Delibes 1987). Conversely, all the fish eaten by L. prouocax in this study were less than 100 mm in length. Similarly, Lejeune (1990) found that 81% of the fish eaten by L. maculicollis in Rwanda were less than 100 mm long. However, scats from southern river otters living permanently in a marine habitat contained 75% fish and 62% crustaceans (relative frequency) (Sielfeld 1984). Therefore, the low frequency of fish in the diet recorded in this study may be the result of habitats with poor fish availability. Otter hunting success is influenced by prey availability, water depth and prey vulnerability (prey size) (Mason & Macdonald 1986, Kruuk 1995). This may explain the small size of fish eaten by southern river otter, and the greater frequency of trout remains found in scats collected at rivers compared with those collected at lake habitats. Most fish length recorded in these habitats were 42 mm for P. gillissi, 72 mm for P. trucha and 21 mm for young trout (Campos 1985). These fish are slower than trout over 100 mm in length (Bainbridge 1958). Furthermore the studied rivers have more shallow areas and ponds than the studied lakes (Campos et al. 1981, 1990, H. Campos, pers. comm.). Prey seasonality Crustaceans and fish are assumed to be more active in the warmer months, so seasonal variations in occurrence in the otter's diet may be expected (Rowe-Rowe
7 Southern river otter diet in Chile ). However, in this study crustaceans and most species of fish were eaten by otters throughout the year without any apparent seasonal variation. Comparison between the study sites The present study does not contain any details of prey availability. However, the significant differences between lakes and rivers recorded, along with the heavy dependence of the southern river otter on crustaceans, would suggest there are different habitat conditions. These include water depth, water surface (ha), current, differences in prey availability and vulnerability that may have been affecting the diet of southern river otter. This is also supported by the significant differences in diversity indices between the determined diet of otters from lakes and from their river outlets. All prey species recorded were equally represented by their occurrence in the scats collected from the river outlets (large Even and H' indexes) more than those collected from the lakes sites. Therefore, the seven regions holding southern river otter populations described by Medina (1996) may not be the best habitats for river otter, but otters are found there because there may be no more habitats available due to their destruction and disturbances by human activities (Medina 1996). Acknowledgements: I am grateful to Drs D. T. Rowe-Rowe and H. Kruuk for their valuable comments on the manuscript. I thank members of the Chilean Otter Group of CODEFF (Comité Nacional Pro Defensa de la Fauna y Flora) for their collaboration, especially J. Parra, R. Monsalve, P. Sandoval and K. Falkenhagen for their important help during the field work and scat analyses. Special thanks are also due to the V. Perez Rosales National Park rangers for their help during the field work. This work was part of the otter conservation programme of CODEFF and financed by Project FZS 1104/1990 of the Frankfurt Zoological Society, Help For Threatened Animals. References Adrian M. I. and Delibes M Food habits of the otter (Lutra lutra) in two habitats of the Donana National Park SW Spain. Journal of Zoology, London 212: Bagenal T Methods for assessment of fish production in fresh water. Handbook No. 3. International Biological Program. Third ed. Blackwell Scientific Publications Ltd., Oxford: Bainbridge R The speed of swimming of fish as related to size and to the frequency and amplitude of the tail beat. Experimental Biology 35: Berenson M. L., Levine D. M. and Rindskopf D Applied statistics. A first course. Prentice Hall, New Jersey: Campos H., Steffen W. and Aguero G Morphometrical, physical and chemical limnology of Lake Panguipulli (Valdivia, Chile). Neues Jahrbuch für Geologie und Paläontologie Monatshefte 10: Campos H Distribution of the fishes in the Andean rivers in the South of Chile. Archiv für Hydrobiologie 104: Campos H., Steffen W., Aguero G., Parra O. and Züniga L Limnological study of Lake Todos Los Santos (Chile) Morphometry, physics, chemestry, plankton, and primary productivity. Archiv für Hydrobiologie, Bd. 117: Chehebar C A survey of the Southern river otter Lutra provocax Thomas in Nahuel Huapi National Park, Argentina. Biological Conservation. 32:
8 292 G. Medina Chehébar G, Gallur A., Giannico G., Gotteli M. and Yorio P A survey of the Southern river otter Lutra prouocax in Lanin, Puelo and Los Alerces National Parks, Argentina, and evaluation of its conservation status. Biological Conservation 38: Erlinge S Food studies of captive otter (Lutra lutra L.). Oikos 19: Jara C. G Aegla rostrata n. sp., (Decapoda, Aeglidae), a new freshwater crustacean from Southern Chile. Studies on Neotropical Fauna and Environment 12: Jara C. G Aegla denticulata lacustris, new subspecies, from lake Rupanco, Chile (Crustacea: Decapoda: Anomura: Aeglidae). Proceedings of the Biological Society of Washington 102: Jenkins D. and Harper R. J Ecology of otters in northern Scotland. II. Analysis of otter (Lutra lutra) and mink (Mustela vison) faeces from Deeside, N.E. Scotland in Journal of Animal Ecology 49: Krebs C. J Ecological methodology. Harper Collins, New York: Kruuk H Wild otters. Predation and populations. Oxford University Press, Oxford: Lejeune A Ecologie alimentaire de la loutre (Hydrictis maculicollis) au lac Muhazi, Rwanda. Mammalia 54: Magurran A. E Ecological diversity and its measurement. Croom. Helm, London: Mason C. F. and Macdonald S.M Otters: Ecology and conservation. Cambridge University Press, Cambridge: Medina G The status of the "huillín" (Lutra prouocax) in Chile. Preliminary information on the current situation of population, habitat conditions and illegal trade. [In: Proceedings V International Otter Colloquium, Hankensbüttel. C. Reuther and R. Rochert, eds]. Habitat 6: Medina G Conservation and status of Lutra provocax in Chile. Pacific Conservation Biology 2: Medina G A comparison of the diet and distribution of southern river otter (Lutra prouocax) and mink (Mustela uison) in Southern Chile. Journal of Zoology, London 242: Melquist W. E. and Hornocker M. G Ecology of river otter in west central Idaho. Wildlife Monographs 83: Rowe-Rowe D. T Food ecology of otters in Natal, South Africa. Oikos 28: Rowe-Rowe D. T Status of otters in Africa. [In: Proceedings V International Otter Colloquium, Hankensbüttel. C. Reuther and R. Rochert, eds. Habitat 6: Shannon C. E. and Weaver W The mathematical theory of communication. University of Illinois Press, Urbana. Sielfeld K. W Food habits of the huillín (Lutra prouocax) (Mammalia, Carnívora, Mustelidae) in the marine environment of Austral Chile. Seminario de Investigación para optar al grado de Licenciado en Ciencias. Facultad de Ciencias, Escuela de Ciencias, Universidad Austral de Chile: Thomas O On certain African and South American otters. Annals and Magazine of Natural History, series 8 (1): Toweill D. E Winter food habits of river otter in western Oregon. Journal of Wildlife Management 38: Wise M. H The use of fish vertebrae in scats for estimating prey size of otter and mink. Journal of Zoology, London 192: Wise M. H., Linn I. J. and Kennedy C. R A comparison of the feeding biology of mink Mustela uison and otter Lutra lutra. Journal of Zoology, London 195: Receiued 16 January 1997, accepted 24 June 1998.
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